Omega-3 fatty acid eicospentaenoic acid attenuates MPP+-induced neurodegeneration in fully differentiated human SH-SY5Y and primary mesencephalic cells

Journal of Neurochemistry

Volumn 124, Issue 6, 2013, Pages 855-868

  Luchtman, Dirk W ^a,b   Meng, Qingjia ^a,e   Wang, Xiaofeng ^a   Shao, Di ^a,c   Song, Cai ^a,d  

^a UNIVERSITY OF PRINCE EDWARD ISLAND   (Canada)

^b UNIVERSITY OF ALBERTA   (Canada)

^c DALHOUSIE UNIVERSITY   (Canada)

^d Chinese Acad Engineer Inst for the Devmt of Endangered Medicinal Resource in Southwest of China   (China)

^e Health Food Safety   (China)

Author keywords

eicosapentaenoic acid; MPTP; neurodegeneration; neuroprotection; omega 3; Parkinson's disease

Indexed keywords

1 METHYL 4 PHENYLPYRIDINIUM; BETA ACTIN; BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; CASPASE 3; CATALASE; CYCLOOXYGENASE 2; CYTOCHROME C; CYTOSOLIC PHOSPHOLIPASE A2; GLUTATHIONE PEROXIDASE; ICOSAPENTAENOIC ACID; OMEGA 3 FATTY ACID; PROTEIN BAX; PROTEIN BCL 2; PROTEIN P47; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SUPEROXIDE DISMUTASE;

ANIMAL CELL; ANTIOXIDANT ACTIVITY; ARTICLE; CELL INCLUSION; CELL VIABILITY; CONTROLLED STUDY; DISEASE MODEL; DOWN REGULATION; EMBRYO; ENZYME RELEASE; HUMAN; HUMAN CELL; IN VITRO STUDY; INHIBITION KINETICS; MESENCEPHALON; MITOCHONDRIAL MEMBRANE POTENTIAL; NERVE CELL DEGENERATION; NERVE CELL DIFFERENTIATION; NEUROPROTECTION; NONHUMAN; PARKINSON DISEASE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT;

1-METHYL-4-PHENYLPYRIDINIUM; ANIMALS; CELL DIFFERENTIATION; CELL LINE, TUMOR; CELLS, CULTURED; EICOSAPENTAENOIC ACID; FATTY ACIDS, OMEGA-3; HUMANS; MESENCEPHALON; NEURODEGENERATIVE DISEASES; NEUROPROTECTIVE AGENTS; OXIDATIVE STRESS; RATS; RATS, WISTAR;

PARKINSONIA;

EID: 84874729665     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/jnc.12068     Document Type: Article

References (64)

1. Anantharam V., Kaul S., Song C., Kanthasamy A., and, Kanthasamy A. G., (2007) Pharmacological inhibition of neuronal NADPH oxidase protects against 1-methyl-4-phenylpyridinium (MPP+)-induced oxidative stress and apoptosis in mesencephalic dopaminergic neuronal cells. Neurotoxicology 28, 988-997.
2. Baydyuk M., Nguyen M. T., and, Xu B., (2010) Chronic deprivation of TrkB signaling leads to selective late-onset nigrostriatal dopaminergic degeneration. Exp. Neurol. 228, 118-125.
3. Bedard K., and, Krause K. H., (2007) The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Phys. Rev. 87, 245-313.
4. Bernardo A., and, Minghetti L., (2006) PPAR-gamma agonists as regulators of microglial activation and brain inflammation. Curr. Pharm. Des. 12, 93-109.
5. Bordet R., Ouk T., Petrault O., et al,. (2006) PPAR: a new pharmacological target for neuroprotection in stroke and neurodegenerative diseases. Biochem. Soc. Trans. 34, 1341-1346.
6. Bousquet M., Saint-Pierre M., Julien C., Salem N. Jr, Cicchetti F., and, Calon F., (2008) Beneficial effects of dietary omega-3 polyunsaturated fatty acid on toxin-induced neuronal degeneration in an animal model of Parkinson's disease. FASEB J. 22, 1213-1225.
7. Bousquet M., Gibrat C., Saint-Pierre M., Julien C., Calon F., and, Cicchetti F., (2009) Modulation of brain-derived neurotrophic factor as a potential neuroprotective mechanism of action of omega-3 fatty acids in a parkinsonian animal model. Prog. Neuropsychopharmacol. Biol. Psychiatry 33, 1401-1408.
8. Bousquet M., Calon F., and, Cicchetti F., (2011a) Impact of omega-3 fatty acids in Parkinson's disease. Ageing Res. Rev. 10, 453-463.
9. Bousquet M., Gue K., Emond V., Julien P., Kang J. X., Cicchetti F., and, Calon F., (2011b) Transgenic conversion of omega-6 into omega-3 fatty acids in a mouse model of Parkinson's disease. J. Lipid Res. 52, 263-271.
10. Brill L. B. II, and, Bennett J. P. Jr, (2003) Dependence on electron transport chain function and intracellular signaling of genomic responses in SH-SY5Y cells to the mitochondrial neurotoxin MPP(+). Exp. Neurol. 181, 25-38.
11. Chen C. T., Liu Z., Ouellet M., Calon F., and, Bazinet R. P., (2009) Rapid beta-oxidation of eicosapentaenoic acid in mouse brain: an in situ study. Prostaglandins Leukot. Essent. Fatty Acids 80, 157-163.
12. Cheung Y. T., Lau W.K., Yu M. S., Lai C. S., Yeung S. C., So K. F., and, Chang R. C., (2009) Effects of all-trans-retinoic acid on human SH-SY5Y neuroblastoma as in vitro model in neurotoxicity research. Neurotoxicology 30, 127-135.
13. Clarke S. D., (2000) Polyunsaturated fatty acid regulation of gene transcription: a mechanism to improve energy balance and insulin resistance. Br. J. Nutr. 83 (Suppl 1), S59-S66.
14. Cristõvão A. C., Guhathakurta S., Bok E., Je G., Yoo S. D., Choi D. H., and, Kim Y. S., (2012) NADPH oxidase 1 mediates α- synucleinopathy in Parkinson's disease. NADPH oxidase 1 mediates α-synucleinopathy in Parkinson's disease. J. Neurosci. 32, 14465-14477.
15. Dauer W., and, Przedborski S., (2003) Parkinson's disease: mechanisms and models. Neuron 39, 889-909.
16. Dehmer T., Lindenau J., Haid S., Dichgans J., and, Schulz J. B., (2000) Deficiency of inducible nitric oxide synthase protects against MPTP toxicity in vivo. J. Neurochem. 74, 2213-2216.
17. Delattre A. M., Kiss A., Szawka R. E., et al,. (2010) Evaluation of chronic omega-3 fatty acids supplementation on behavioral and neurochemical alterations in 6-hydroxydopamine-lesion model of Parkinson's disease. Neurosci. Res. 66, 256-264.
18. Dennis J., and, Bennett J. P., (2003) Interactions among nitric oxide and Bcl-family proteins after MPP+ exposure of SH-SY5Y neural cells I: MPP+ increases mitochondrial NO and Bax protein. J. Neurosci. Res. 72, 76-88.
19. Ding Y. X., Xia Y., Jiao X. Y., Duan L., Yu J., Wang X., and, Chen L. W., (2011) The TrkB-positive dopaminergic neurons are less sensitive to MPTP insult in the substantia nigra of adult C57/BL mice. Neurochem. Res. 36, 1759-1766.
20. Drechsel D. A., and, Patel M., (2008) Role of reactive oxygen species in the neurotoxicity of environmental agents implicated in Parkinson's disease. Free Radic. Biol. Med. 44, 1873-1886.
21. Dyall S. C., and, Michael-Titus A. T., (2008) Neurological benefits of omega-3 fatty acids. Neuromolecular Med. 10, 219-235.
22. Ebadi M., Bashir R. M., Heidrick M. L., Hamada F. M., Refaey H. E., Hamed A., Helal G., Baxi M. D., Cerutis D. R., and, Lassi N. K., (1997) Neurotrophins and their receptors in nerve injury and repair. Neurochem. Int. 30, 347-374.
23. Fath T., Ke Y. D., Gunning P., Götz J., and, Ittner L. M., (2009) Primary support cultures of hippocampal and substantia nigra neurons. Nat. Protoc. 4, 78-85.
24. Hoang T., Choi D. K., Nagai M., et al,. (2009) Neuronal NOS and cyclooxygenase-2 contribute to DNA damage in a mouse model of Parkinson disease. Free Radic. Biol. Med. 47, 1049-1056.
25. Kalivendi S. V., Cunningham S., Kotamraju S., Joseph J., Hillard C. J., and, Kalyanaraman B., (2004) Alpha-synuclein up-regulation and aggregation during MPP+-induced apoptosis in neuroblastoma cells: intermediacy of transferrin receptor iron and hydrogen peroxide. J. Biol. Chem. 279, 15240-15247.
26. Kawashima A., Harada T., Kami H., Yano T., Imada K., and, Mizuguchi K., (2010) Effects of eicosapentaenoic acid on synaptic plasticity, fatty acid profile and phosphoinositide 3-kinase signaling in rat hippocampus and differentiated PC12 cells. J. Nutr. Biochem. 21, 268-277.
27. Kitajka K., Sinclair A. J., Weisinger R. S., Weisinger H. S., Mathai M., Jayasooriya A. P., Halver J. E., and, Puskás L. G., (2004) Effects of dietary omega-3 polyunsaturated fatty acids on brain gene expression. Proc. Natl Acad. Sci. USA 101, 10931-10936.
28. Klivenyi P., Beal M. F., Ferrante R. J., Andreassen O. A., Wermer M., Chin M. R., and, Bonventre J. V., (1998) Mice deficient in group IV cytosolic phospholipase A2 are resistant to MPTP neurotoxicity. J. Neurochem. 71, 2634-2637.
29. Kou W., Luchtman D., and, Song C., (2008) Eicosapentaenoic acid (EPA) increases cell viability and expression of neurotrophin receptors in retinoic acid and brain-derived neurotrophic factor differentiated SH-SY5Y cells. Eur. J. Nutr. 47, 104-113.
30. Langelier B., Alessandri J. M., Perruchot M. H., Guesnet P., and, Lavialle M., (2005) Changes of the transcriptional and fatty acid profiles in response to n-3 fatty acids in SH-SY5Y neuroblastoma cells. Lipids 40, 719-728.
31. Lawson L. J., Perry V. H., Dri P., and, Gordon S., (1990) Heterogeneity in the distribution and morphology of microglia in the normal adult mouse brain. Neuroscience 39, 151-170.
32. Lonergan P. E., Martin D. S., Horrobin D. F., and, Lynch M. A., (2002) Neuroprotective effect of eicosapentaenoic acid in hippocampus of rats exposed to gamma-irradiation. J. Biol. Chem. 277, 20804-20811.
33. Lonergan P. E., Martin D. S., Horrobin D. F., and, Lynch M. A., (2004) Neuroprotective actions of eicosapentaenoic acid on lipopolysaccharide-induced dysfunction in rat hippocampus. J. Neurochem. 91, 20-29.
34. Luchtman D. W., and, Song C., (2010) Why SH-SY5Y cells should be differentiated. Neurotoxicology 31, 164-165.
35. Luchtman D. W., Meng Q., and, Song C., (2012) Ethyl-eicosapentaenoate (E-EPA) attenuates motor impairments and inflammation in the MPTP-probenecid mouse model of Parkinson's disease. Behav. Brain Res. 226 (2), 386-396.
36. Luellen B. A., Szapacs M. E., Materese C. K., and, Andrews A. M., (2006) The neurotoxin 2'-NH2-MPTP degenerates serotonin axons and evokes increases in hippocampal BDNF. Neuropharmacology 50, 297-308.
37. Mao L., and, Wang J. Q., (2003) Group I metabotropic glutamate receptor-mediated calcium signalling and immediate early gene expression in cultured rat striatal neurons. Eur. J. Neurosci. 17, 741-750.
38. Marttila R. J., Lorentz H., and, Rinne U. K., (1988) Oxygen toxicity protecting enzymes in Parkinson's disease. Increase of superoxide dismutase-like activity in the substantia nigra and basal nucleus. J. Neurol. Sci. 86, 321-331.
39. McGeer P. L., and, McGeer E. G., (2008) Glial reactions in Parkinson's disease. Mov. Disord. 23, 474-483.
40. Meng Q., Luchtman D. W., El Bahh B., Zidichouski J. A., Yang J., and, Song C., (2010) Ethyl-eicosapentaenoate modulates changes in neurochemistry and brain lipids induced by parkinsonian neurotoxin 1-methyl-4-phenylpyridinium in mouse brain slices. Eur. J. Pharmacol. 649, 127-134.
41. Mogi M., Togari A., Kondo T., Mizuno Y., Komure O., Kuno S., Ichinose H., and, Nagatsu T., (1999) Brain-derived growth factor and nerve growth factor concentrations are decreased in the substantia nigra in Parkinson's disease. Neurosci. Lett. 270, 45-48.
42. Nakamura K., Bindokas V. P., Marks J. D., Wright D. A., Frim D. M., Miller R. J., and, Kang U. J., (2000) The selective toxicity of 1-methyl-4-phenylpyridinium to dopaminergic neurons: the role of mitochondrial complex I and reactive oxygen species revisited. Mol. Pharmacol. 58, 271-278.
43. Offen D., Beart P. M., Cheung N. S., Pascoe C. J., Hochman A., Gorodin S., Melamed E., Bernard R., and, Bernard O., (1998) Transgenic mice expressing human Bcl-2 in their neurons are resistant to 6-hydroxydopamine and 1-methyl-4-phenyl-1,2,3,6- tetrahydropyridine neurotoxicity. Proc. Natl Acad. Sci. USA 95, 5789-5794.
44. Peet M., Brind J., Ramchand C. N., Shah S., and, Vankar G. K., (2010) Schizophr. Res. 49, 243-251.
45. Presgraves S. P., Ahmed T., Borwege S., and, Joyce J. N., (2004) Terminally differentiated SH-SY5Y cells provide a model system for studying neuroprotective effects of dopamine agonists. Neurotox. Res. 5, 579-598.
46. Rao J. S., Ertley R. N., Lee H. J., DeMar J. C. Jr, Arnold J. T., Rapoport S. I., and, Bazinet R. P., (2007a) N-3 polyunsaturated fatty acid deprivation in rats decreases frontal cortex BDNF via a p38 MAPK-dependent mechanism. Mol. Psychiatry 12, 36-46.
47. Rao J. S., Ertley R. N., DeMar J. C. Jr, Rapoport S. I., Bazinet R. P., and, Lee H. J., (2007b) Dietary n-3 PUFA deprivation alters expression of enzymes of the arachidonic and docosahexaenoic acid cascades in rat frontal cortex. Mol. Psychiatry 12, 151-157.
48. Rezak M., (2007) Current pharmacotherapeutic treatment options in Parkinson's disease. Dis. Mon. 53, 214-222.
49. Schapira A. H., (2010) Complex I: inhibitors, inhibition and neurodegeneration. Exp. Neurol. 224, 331-335.
50. Song C., Zhang X. Y., and, Manku M., (2009) Increased phospholipase A2 activity and inflammatory response but decreased nerve growth factor expression in the olfactory bulbectomized rat model of depression: effects of chronic ethyl-eicosapentaenoate treatment. J. Neurosci. 29, 14-22.
51. Sere Y. Y., Reqnacq M., Colas J., and, Berges T., (2010) A Saccharomyces cerevisiae strain unable to store neutral lipids is tolerant to oxidative stress induced by α-synuc. Free Radic. Biol. Med. 49, 1755-1764.
52. Szabo S. E., Monroe S. L., Fiorino S., Bitzan J., and, Loper K., (2004) Evaluation of an automated instrument for viability and concentration measurements of cryopreserved hematopoietic cells. Lab. Hematol. 10, 109-111.
53. Taepavarapruk P., and, Song C., (2010) Reductions of acetylcholine release and nerve growth factor expression are correlated with memory impairment induced by interleukin-1beta administrations: effects of omega-3 fatty acid EPA treatment. J. Neurochem. 112, 1054-1064.
54. Teismann P., Tieu K., Choi D. K., Wu D. C., Naini A., Hunot S., Vila M., Jackson-Lewis V., and, Przedborski S., (2003) Cyclooxygenase-2 is instrumental in Parkinson's disease neurodegeneration. Proc. Natl Acad. Sci. USA 100, 5473-5478.
55. Thomas B., Saravanan K. S., and, Mohanakumar K. P., (2008) In vitro and in vivo evidences that antioxidant action contributes to the neuroprotective effects of the neuronal nitric oxide synthase and monoamine oxidase-B inhibitor, 7-nitroindazole. Neurochem. Int. 52, 990-2001.
56. de la Torre M. R., Casado A., Lõpez-Fernández M. E., Carrascosa D., Casado M. C., Venarucci D., and, Venarucci V., (1996) Human aging brain disorders: role of antioxidant enzymes. Neurochem. Res. 21, 885-888.
57. Vila M., Jackson-Lewis V., Vukosavic S., Djaldetti R., Liberatore G., Offen D., Korsmeyer S. J., and, Przedborski S., (2001) Bax ablation prevents dopaminergic neurodegeneration in the 1-methyl- 4-phenyl-1,2,3,6- tetrahydropyridine mouse model of Parkinson's disease. Proc. Natl Acad. Sci. USA 98, 2837-2842.
58. Von Bohlen und Halbach O., Minichiello L., and, Unsicker K., (2005) Haploinsufficiency for trkB and trkC receptors induces cell loss and accumulation of alpha-synuclein in the substantia nigra. FASEB J. 19, 1740-1742.
59. Wang T., Pei Z., Zhang W., Liu B., Langenbach R., Lee C., Wilson B., Reece J. M., Miller D. S., and, Hong J. S., (2005) MPP+-induced COX-2 activation and subsequent dopaminergic neurodegeneration. FASEB J. 19, 1134-1136.
60. Wu D. C., Teismann P., Tieu K., Vila M., and, Jackson-Lewis V., (2003) NADPH oxidase mediates oxidative stress in the 1-methyl-4-phenyl-1,2,3,6- tetrahydropyridine model of Parkinson's disease. Proc. Natl Acad. Sci. USA 100, 6145-6150.
61. Xie H. R., Hu L. S., and, Li G. Y., (2010) SH-SY5Y human neuroblastoma cell line: in vitro cell model of dopaminergic neurons in Parkinson's disease. Chin. Med. J. 123, 1086-1092.
62. Youdim K. A., Martin A., and, Joseph J. A., (2000) Essential fatty acids and the brain: possible health implications. Int. J. Dev. Neurosci. 18, 383-399.
63. Zawada W. M., Banninger G. P., Thornton J., Marriott B., Cantu D., Rachubinski A. L., Das M., Griffin W. S., and, Jones S. M., (2011) Generation of reactive oxygen species in 1-methyl-4-phenylpyridinium (MPP+) treated dopaminergic neurons occurs as an NADPH oxidase-dependent two-wave cascade. J. Neuroinflammation 8, 129. doi: 10.1186/1742-2094-8-129.
64. Zeevalk G. D., Manzino L., Sonsalla P. K., and, Bernard L. P., (2007) Characterization of intracellular elevation of glutathione (GSH) with glutathione monoethyl ester and GSH in brain and neuronal cultures: relevance to Parkinson's disease. Exp. Neurol. 20, 512-552.